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Octopus, Squid Genome Assemblies Reveal Hallmarks of Cephalopod Evolution

Atlantic longfin inshore squid

NEW YORK – Large rearrangements in the ancestral cephalopod genome appear to have contributed to the evolution of the complex behaviors and large nervous systems that mark the lineage, according to new research.

The results come from an analysis of the genomes of octopus and squid species by researchers in the US, Austria, and Japan, published on Wednesday in Nature Communications.

"By understanding the cephalopod genome, we can gain insight into the genes that are important in setting up the nervous system, as well as into neuronal function," co-first and co-corresponding author Caroline Albertin, a researcher at the Woods Hole Marine Biological Laboratory, said in a statement.

Using Pacific Biosciences long-read sequencing, Illumina short reads, and HiC chromosome interaction profiles, the scientists put together a chromosome-level genome assembly for the Atlantic longfin inshore squid, or Boston market squid (Doryteuthis pealeii), that contained more than 24,900 predicted protein-coding genes, along with transcriptome sequences spanning more than two dozen tissues.

When the team analyzed the 4.6 gigabase D. pealeii genome assembly alongside improved genome assemblies for other members of the soft-bodied or "coleoid" cephalopod group — the California two-spot octopus (Octopus bimaculoides) and the Hawaiian bobtail squid (Euprymna scolopes) — it saw rampant genome reshuffling.

"Large and elaborate brains have evolved a couple of times. One famous example is the vertebrates. Another is the soft-bodied cephalopods, which serve as a separate example for how a large and complicated nervous system can be put together," Albertin said, noting that chromosome-level assemblies "allowed us to better refine what genes are there and what their order is, because the genome is less fragmented."

Based on their comparative analyses, the researchers suggested that early cephalopod evolution was marked by genome reorganization and rearrangements compared to sequences in non-cephalopod mollusks, together with expansions or duplications affecting brain development-related gene sets, protocadherin genes, and gene families specific to cephalopods.

"[I]n cephalopods, the genome has gone through bursts of restructuring. This presents an interesting situation: Genes are put into new locations in the genome, with new regulatory elements driving the genes' expression," Albertin said, noting that such shuffling "might create opportunities for novel traits to evolve."

For his part, co-senior and co-corresponding author Clifton Ragsdale, a researcher at the University of Chicago, noted that while genome duplications contributed to vertebrate evolution, "the evolution of soft-bodied cephalopods involved similarly massive genome changes, but the changes are not whole-genome duplications but rather immense genome rearrangements, as if the ancestral genomes were put in a blender."

Finally, the team pointed out that the cephalopod sequences also contained shifts in messenger RNA editing patterns. These included mRNA editing features specific to neural tissue, along with RNA editing shifts in noncoding repetitive element sequences.

"This catalog of editing across different tissues provides a resource to ask follow-up questions about the effects of the editing," Albertin said.

In a related study published in Nature Communications in April, members of the same team outlined gene expression and regulatory features found in the Hawaiian bobtail squid (E. scolopes) with a combination of chromosomal conformation capture, ATAC-seq-based open chromatin profiling, RNA sequencing, and other approaches.

"Together, these data allow us to gain insights into the impact of evolutionary changes in gene linkages and the emergence of novel gene regulation," the authors reported, noting that the work "provides the basis for the understanding of the evolution of cephalopod genomes and possible implications on morphological novelties in this clade."